Amro Zayed

Genomic signatures of evolutionary transitions from solitary to group living

For bees, many roads lead to social harmony Eusociality, where workers sacrifice their reproductive rights to support the colony, has evolved repeatedly and represents the most evolved form of social evolution in insects. Kapheim et al. looked across the genomes of 10 bee species with varying degrees of sociality to determine the underlying genomic contributions. No one genomic path led to eusociality, but similarities across genomes were seen in features such as increases in gene regulation and methylation. It also seems that selection pressures relaxed after the emergence of complex sociality. Science, this issue p. 1139 Social evolution in bees has followed diverse genomic paths but shares genomic patterns. The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Significance Most hypotheses explaining the evolution of sociality in insects assume that positive selection drives the evolution of worker traits. Yet we know little about the extent of natural selection acting on social insects. We produced a map of positive selection for the honey bee through analysis of 40 individual genomes. We found strong evidence of positive selection acting on genes and regulatory sequences, and we discovered that mutations in worker-biased proteins tend to have greater fitness effects than mutations in queen-biased proteins. We also found many instances of positive selection acting on genes that influence worker traits, suggesting that worker phenotypes represent a major vector for adaptation in social insects. Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea- and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.

Understanding the Relationship Between Brain Gene Expression and Social Behavior: Lessons from the Honey Bee

Behavior is a complex phenotype that is plastic and evolutionarily labile. The advent of genomics has revolutionized the field of behavioral genetics by providing tools to quantify the dynamic nature of brain gene expression in relation to behavioral output. The honey bee Apis mellifera provides an excellent platform for investigating the relationship between brain gene expression and behavior given both the remarkable behavioral repertoire expressed by members of its intricate society and the degree to which behavior is influenced by heredity and the social environment. Here, we review a linked series of studies that assayed changes in honey bee brain transcriptomes associated with natural and experimentally induced changes in behavioral state. These experiments demonstrate that brain gene expression is closely linked with behavior, that changes in brain gene expression mediate changes in behavior, and that the association between specific genes and behavior exists over multiple timescales, from physiological to evolutionary.

Successful Biological Invasion despite a Severe Genetic Load

Understanding the factors that influence the success of ecologically and economically damaging biological invasions is of prime importance. Recent studies have shown that invasive populations typically exhibit minimal, if any, reductions in genetic diversity, suggesting that large founding populations and/or multiple introductions are required for the success of biological invasions, consistent with predictions of the propagule pressure hypothesis. Through population genetic analysis of neutral microsatellite markers and a gene experiencing balancing selection, we demonstrate that the solitary bee Lasioglossum leucozonium experienced a single and severe bottleneck during its introduction from Europe. Paradoxically, the success of L. leucozonium in its introduced range occurred despite the severe genetic load caused by single-locus complementary sex-determination that still turns 30% of female-destined eggs into sterile diploid males, thereby substantially limiting the growth potential of the introduced population. Using stochastic modeling, we show that L. leucozonium invaded North America through the introduction of a very small number of propagules, most likely a singly-mated female. Our results suggest that chance events and ecological traits of invaders are more important than propagule pressure in determining invasion success, and that the vigilance required to prevent invasions may be considerably greater than has been previously considered.

Use of diploid male frequency data as an indicator of pollinator decline

Pollination deficits in agricultural and natural systems are suggestive of large reductions in pollinator populations. However, actual declines are difficult to demonstrate using census data. Here, we show census data to be misleading because many abundant pollinators exhibit high levels of production of sterile diploid males usually found only in small inbred hymenopteran populations; Euglossa imperialis exhibits high levels of diploid male production induced by low effective population sizes (Ne ≈ 15), despite being the most abundant orchid bee in lowland tropical forests in Panama. We caution that although some pollinators appear abundant on the basis of census data, their long–term persistence may be highly tenuous based on genetic evidence. We propose the use of diploid male frequency data as a metric for assessing the sustainability of bee populations.

Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation

Oligolectic bees are specialists that collect pollen from one or a few closely related species of plants, while polylectic bees are generalists that collect pollen from both related and unrelated species of plants. Because of their more restricted range of floral hosts, it is expected that specialists persist in more isolated populations than do generalists. We present data on the population structure of two closely related bee species sampled from a super abundant floral host in the southern Atacama Desert. Pairwise comparisons of population subdivision over identical distances revealed that the specialist bee had significantly more differentiated populations in comparison to the generalist. Further, populations of the specialist had significantly less genetic variation, measured as observed and expected heterozgyosity, than those of the generalist. Our data support the hypothesis of decreased gene flow among populations of the specialist bee even at equivalent geographic distances. The resulting reductions in effective population size for specialists make them particularly prone to extinction due to both demographic and genetic reasons. Our findings have important implications for the conservation of bees and other specialist insects.

Management increases genetic diversity of honey bees via admixture

The process of domestication often brings about profound changes in levels of genetic variation in animals and plants. The honey bee, Apis mellifera, has been managed by humans for centuries for both honey and wax production and crop pollination. Human management and selective breeding are believed to have caused reductions in genetic diversity in honey bee populations, thereby contributing to the global declines threatening this ecologically and economically important insect. However, previous studies supporting this claim mostly relied on population genetic comparisons of European and African (or Africanized) honey bee races; such conclusions require reassessment given recent evidence demonstrating that the honey bee originated in Africa and colonized Europe via two independent expansions. We sampled honey bee workers from two managed populations in North America and Europe as well as several old-world progenitor populations in Africa, East and West Europe. Managed bees had highly introgressed genomes representing admixture between East and West European progenitor populations. We found that managed honey bees actually have higher levels of genetic diversity compared with their progenitors in East and West Europe, providing an unusual example whereby human management increases genetic diversity by promoting admixture. The relationship between genetic diversity and honey bee declines is tenuous given that managed bees have more genetic diversity than their progenitors and many viable domesticated animals.

Chronic exposure to neonicotinoids reduces honey bee health near corn crops

Damage confirmed Early studies of the impacts of neonicotinoid insecticides on insect pollinators indicated considerable harm. However, lingering criticism was that the studies did not represent field-realistic levels of the chemicals or prevailing environmental conditions. Two studies, conducted on different crops and on two continents, now substantiate that neonicotinoids diminish bee health (see the Perspective by Kerr). Tsvetkov et al. find that bees near corn crops are exposed to neonicotinoids for 3 to 4 months via nontarget pollen, resulting in decreased survival and immune responses, especially when coexposed to a commonly used agrochemical fungicide. Woodcock et al., in a multicounty experiment on rapeseed in Europe, find that neonicotinoid exposure from several nontarget sources reduces overwintering success and colony reproduction in both honeybees and wild bees. These field results confirm that neonicotinoids negatively affect pollinator health under realistic agricultural conditions. Science, this issue p. 1395, p. 1393; see also p. 1331 Bee health is affected by neonicotinoids under field-realistic conditions across crops conditions. Experiments linking neonicotinoids and declining bee health have been criticized for not simulating realistic exposure. Here we quantified the duration and magnitude of neonicotinoid exposure in Canada’s corn-growing regions and used these data to design realistic experiments to investigate the effect of such insecticides on honey bees. Colonies near corn were naturally exposed to neonicotinoids for up to 4 months—the majority of the honey bee’s active season. Realistic experiments showed that neonicotinoids increased worker mortality and were associated with declines in social immunity and increased queenlessness over time. We also discovered that the acute toxicity of neonicotinoids to honey bees doubles in the presence of a commonly encountered fungicide. Our work demonstrates that field-realistic exposure to neonicotinoids can reduce honey bee health in corn-growing regions.

Recombination is associated with the evolution of genome structure and worker behavior in honey bees

The rise of insect societies, marked by the formation of reproductive and sterile castes, represents a major unsolved mystery in evolution. Across several independent origins of sociality, the genomes of social hymenopterans share two peculiar attributes: high recombination and low but heterogeneous GC content. For example, the genome of the honey bee, Apis mellifera, represents a mosaic of GC-poor and GC-rich regions with rates of recombination an order of magnitude higher than in humans. However, it is unclear how heterogeneity in GC content arises, and how it relates to the expression and evolution of worker traits. Using population genetic analyses, we demonstrate a bias in the allele frequency and fixation rate of derived C or G mutations in high-recombination regions, consistent with recombination’s causal influence on GC-content evolution via biased gene conversion. We also show that recombination and biased gene conversion actively maintain the heterogeneous GC content of the honey bee genome despite an overall A/T mutation bias. Further, we found that GC-rich genes and intergenic regions have higher levels of genetic diversity and divergence relative to GC-poor regions, also consistent with recombination’s causal influence on the rate of molecular evolution. Finally, we found that genes associated with behavior and those with worker-biased expression are found in GC-rich regions of the bee genome and also experience high rates of molecular evolution. Taken together, these findings suggest that recombination acts to maintain a genetically diverse and dynamic part of the genome where genes underlying worker behavior evolve more quickly.

High levels of diploid male production in a primitively eusocial bee (Hymenoptera: Halictidae)

Under single locus complementary sex determination (sl-CSD), diploid males are produced from fertilized eggs that are homozygous at the sex-determining locus. Diploid males are effectively sterile, and thus their production generates a costly genetic load. Using allozyme electrophoresis, a large number of diploid males were detected in natural populations of the primitively eusocial bee, Halictus poeyi Lepeletier collected in southern and central Florida during May 2000. Estimates for the proportion of diploids that are male ranged from 9.1% to 50%, while the frequency of matched matings ranged from 18.2% to 100%. The effective number of alleles at the sex-determining locus ranged from two to 11, with an average of five alleles. The effective population size of Halictus poeyi was estimated to be 19.6 ± 2.5 SE. These data are interpreted in the light of the biogeographic history of Florida and the social biology/population dynamics of H. poeyi.